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Original article

Sensorimotor contribution to shoulder stability: Effect ofinjury and rehabilitation*

Joseph B. Myers*, Craig A~ Wassinger, Scott M. Lephart

Department (if Sports Medicine and Nutrition. Neuromuscular Re.l'earch Laboratory. School of Health and Rehabilitation Science.l'.UPMC Center for Sports Medicine. University of Pittsburgh. 3200 South Water Street. Pitt.l'burgh. PA 15203. USA

Received 27 October 2005; accepted 6 April 2006

Abstract

Shoulder joint stability is the humeral head remaining or promptly returning to proper alignment within the glenoid fossa. This ismediated by both mechanical and dynamic restraint mechanisms. CoOJdination of these restraint systems is required for shoulderjoint stability, The sensorimotor system is defined as al1 of the sensory, motor, and central integration and processing componentsinvolved in maintaining joint stability, The sensorimotor system is comprised of several components including proprioception, jointposition sense, kinesthesia, sensation of force, and neuromuscular control. With joint injury, not only are the mechanical restraintsdisrupted Goint capsule, glenoid labrum, etc.) but also, the sensorimotor system is affected. Restoration of the sensorimotor systemhas been shown to occur through both surgical and conservative intervention and rehabilitation. Surgery has been shown to restoreboth mechanical restraints and the sensorimotor system. Specific rehabilitation techniques have also been effective at improving thesensorimotor system in healthy and pathological patients,~ 2006 Elsevier Ltd. Al1 rights reserved,

KeYlvords: Proprioception; Neuromuscular control; Joint stability

1. Introduction activation and force production by the muscles sur-rounding the shoulder.

Stability is defined as the state of remaining un- Functional joint stability is defined as possessingchanged, even in the presence of forces that would adequate stability to perform functional activity andnormally change the state or condition (Thomas, 1993). results from the interaction between the mechanical andApplying this definition to the shoulder, glenohumeral dynamic restraints mentioned above (Lephart et al.,stability is the state of the humeral head remaining or 2000). As separate entities, neither the mechanical norpromptly returning to proper alignment within the dynamic restraints can act alone in providing functionalglenoid fossa through an equalization of forces. Joint joint stability, but requires a mechanical-dynamicstability is mediated by both mechanical and dynamic restraint interaction to achieve a stable shoulder. Thisrestraints. Mechanical restraints include the glenohum- mechanical-dynamic restraint interaction is mediated byeral joint capsule, glenohumeral and extracapsular the sensorimotor system.ligaments, glenoid labrum, bony geometry and intra-articular pressure. Dynamic restraint results from

2. Sensorimotor system

"'Presented at: 2nd International Conference on Movement Th . t t .d fi d II f th' ,. e sensonmo or sys em IS e ne as a 0 eDysfunction, pam, and performance: Evidence and effect, ...

"Corresponding author, Tel,: 4124323800; fax: 4124323801, sensory, motor, and central integration and processingE-mail address: myersjb@upmc,edu (J,B, Myers), components involved in maintaining joint stability

I 356-689Xj$ -see front matter it) 2006 Elsevier Ltd, All rights reserved,doi:IO, 1016jj,math,2006,04,002

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198 J.B. Myers et al. / Manua./ Therap.v II (2006) 197-201

(Riemann and Lephart, 2002a, b). For example, the whether caused by a traumatic or atraumatic mechan-mechanical restraints about the shoulder not only ism, results in mechanical instability. Accompanyingprovide physical restraint to the humeral head, but also physical disruption of the mechanical stabilizers iscontribute to stability by providing neural feedback decreased capsuloligamentous-musculotendinous me-(proprioception) to the central nervous system (CNS) chanoreceptor stimulation thus altering the sensorimo-where it is integrated with other somatosensory, tor contribution to dynamic restraint and joint stabilityvestibular, and visual input, and ultimately results in (Lephart and Henry, 1996). This combination ofthe generation of efferent control over the dynamic mechanical deficits and sensorimotor alterations con-restraints about the shoulder joint (neuromuscular tribute to deficits in functional stability (Lephart and jcontrol). Proprioception is defined as the afferent Henry, 1996). Ultimately, the deficient function mayinformation, arising from peripheral areas of the body contribute to reinjury patterns often seen at the shoulder(including the mechanical and dynamic restraints about joint. For example, with an acute glenohumeralthe shoulder) that contributes to joint stability, postural dislocation-subluxation, the mechanical restraints in-control, and motor control (Lephart et al., 2000; cluding glenohumeral joint capsule, glenohumeralliga-Riemann and Lephart, 2002a, b). Proprioception has ments, and glenoid labrum are compromised. Yet withinthree submodalities including joint position sense, those structures are mechanoreceptors that contributekinesthesia, and sensation of force (Riemann and proprioeceptive information to the sensorimotor systemLephart, 2002a, b). Joint position sense is the apprecia- that ultimately provides neuromuscular control over thetion and interpretation of information concerning one's dynamic restraints about the shoulder. Thus with jointjoint position and orientation in space. Kinesthesia is injury, not only are the mechanical restraints affected,the ability to appreciate and interpret joint motions but also the sensorimotor contribution to dynamic(Myers and Lephart, 2000). Sensation of force is the ~t,ability is affected.ability to appreciate and interpret force applied to or Several studies have shown that instability at thegenerated within a joint (Myers and Lephart, 2000). shoulder has deleterious effects on proprioceptionProprioceptive information originates at the level of the (Smith and Brunolli, 1989; Lephart et al., 1994;mechanoreceptor. Mechanoreceptors are peripheral Zuckerman et al., 2003; Barden et al., 2004). Both jointafferent sensory neurons present within muscle, tendons, position sense and kinesthesia are altered in patientsfascia, joint capsule, ligaments, and skin about a joint diagnosed with glenohumeral instability (Smith and(Kikuchi, 1968; Grigg, 1994; Vangsness et al., 1995). Brunolli, 1989; Lephart et al., 1994; Zuckerman et al.,Mechanoreceptors are mechanically sensitive receptors 2003; Barden et al., 2004). Accompanying the disruptionthat transduce mechanical tissue deformation as fre- of the mechanical stabilizing structures, it is believedquency modulated neural signals to the central nervous that decreased capsuloligamentous mechanoreceptorsystem (CNS) through afferent sensory pathways stimulation resulting from tissue deafferentation and/(Grigg, 1994). Mechanoreceptors including pacinian or the increased tissue laxity limiting mechanoreceptorscorpuscles, ruffini endings, golgi tendon organs, and stimulation, thus decreasing proprioception (Lephartmuscle spindles have been identified at the shoulder and Henry, 1996; Tibone et al., 1997). Barden et al.(Vangsness et al., 1995; Solomonow et al., 1996; Gohlke (2004) demonstrated errors bilaterally in joint positionet al., 1996; Ide et al., 1996; Gohlke et al., 1998). sense in subjects exhibiting unilateral instability. These

Neuromuscular control is the subconscious activation results suggest that alterations in the central processingof the dynamic restraints about the shoulder in prepara- mechanisms may also be present. Interestingly, Tibonetion and in response to joint motion and loading for the et al. (1997) reported that no significant differencespurpose of maintaining joint stability (Myers and existed between normal subjects and subjects withLephart, 2000). These neuromuscular control mechanisms instability, using cortical evoked potential. Given thatinclude coordinated muscle activation during functional joint capsule mechanoreceptors were stimulated withtasks, coactivation of the shoulder musculature (force electrical potentials rather then tissue deformation, thesecoupling), muscular reflexes, and regulation of muscle results suggest that capsular laxity alone rather thantone and stiffness (Myers and Lephart, 2000, 2002). The mechanoreceptor trauma resulting in deafferentation isforces provided by the muscles about the shoulder responsible for proprioception deficits.maintain centralization of the humeral head within the Proprioceptive deficits have also been identified inglenoid while still allowing for a high degree of mobility. patients diagnosed with osteoarthritis (Cuomo et al.,

2005). Proprioceptive deficits were attributed to de-creases in shoulder muscle activity levels combined with

3. The effects of injury on the sensorimotor system local muscle atrophy (Cuomo et al., 2005). Additionally,the increased afferent signals sent by pain receptors

Injury to the stabilizing structures of the shoulder about the shoulder were believed to override and(capsuloligamentous, articular, and musculotendinous) subsequently decrease proprioception afferents. The

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J.B. Myer.l'etal. / Manual Therapy II (2006) 197-201 199

I

work by Safran et al. (200 I) supports the role of pain in mance compared to both asymptomatic and normaladversely affecting proprioception. These results de- subjects. Our laboratory recently identified that patientsmonstrated that throwers with shoulder pain have with subacromial impingement exhibited less subscapu-decreased proprioception most likely due to increased laris-infraspinatus, supraspinatus-subscapularis, andnociceptor activity in the painful shoulder of baseball supraspinatus-infraspinatus coactivation (Myers et al.,players Safran et al. (200 I). Subacromial impingement 2003). Increased middle deltoid and latissimus dorsihas also been linked to proprioceptive deficits. Machner activity was exhibited by the impingement patients. Theet al. (2003) demonstrated decreased kinesthesia in results indicate that patients with subacromial impinge-subjects diagnosed with unilateral stage II subacromial ment exhibit suppressed rotator cuff coactivation andimpingement. The authors theorized that the subacro- abnormal humeral mover alterations during humeralmial bursa was deficient in relaying the movement sense elevation. These demonstrated muscle activation altera-signals (Machner et al., 2003). tions may contribute to impingement of the subacromial

Given the proprioceptive deficits associated with structures and subsequent pain during overhead eleva-shoulder joint injury, neuromuscular control is hypothe- tion in patients with subacromial impingement.sized to be altered as well (Myers and Lephart, 2000,2002). Several investigators have assessed the neuro-muscular control component of dynamic joint stability 4. Sensorimotor restorationin subjects presenting with glenohumeral instability .(Glousman et al., 1988; Kronberg et al., 1991; McMa- There is evidence to suggest that the sensorimotorhon et al., 1996; Myers et al., 2004). Muscle activation contributors to joint stability can be restored. Foralterations were identified in patients with glenohumeral example, surgical intervention to restore mechanicalinstability during both simple elevation tasks (Kronberg st,;,:~ility has a demonstrated benefit in restoringet al., 1991; McMahon et al., 1996) and while throwing a proprioception (Lephart et al., 1994, 2002; Zuckermanbaseball (Glousman et al., 1988). Deficits in coactivation et al., 2003; Potzl et al., 2004; Cuomo et al., 2005). Theof the rotator cuff and primary humeral movers were main goal of surgery for glenohumeral instability is topresent, possibly leading to compromised dynamic joint reestablish mechanical restraint to the humeral head.stability and further exacerbating the existing instabiJity. Yet as reported by several investigators, the surgery wasOur laboratory recently assessed reflexive characteristics also successful at restoring proprioception (Lephartof the shoulder muscles in patients diagnosed with et al., 1994, 2002; Zuckerman et al., 2003; Potzl et al.,anterior glenohumeral instability (Myers et al., 2004). 2004; Cuomo et al., 2005). It is believed that byThe patients with instability demonstrated suppressed reestablishing tension with the glenohumeral jointpectoralis major and biceps brachii mean reflexive capsule and ligaments, that mechanoreceptor stimula-activation, significantly slower biceps brachii reflex tion is also reestablished (Lephart et al., 1994, 2002;latency, and suppressed supraspinatus-subscapularis Zuckerman et al., 2003; Potzl et al., 2004; Cuomo et al.,coactivation. The results suggested that in addition to 2005). Mechanoreceptors may also repopulate the jointthe capsuloligamentous deficiency and proprioceptive capsule allowing reinnervation following surgery as adeficits present in patients with anterior glenohumeral normal part of the histological healing process (Lephartinstability, muscle activation alterations are also pre- et al., 1994, 2002). Potzl et al. (2004) found an increasesent. The suppressed rotator cuff coactivation, slower in proprioception bilaterally following unilateral surgi-biceps brachii activation, and decreased pectoralis major cal intervention, thus hypothesizing an alteration inand biceps brachii mean activation may contribute to central mediation of proprioception may also contributethe recurrent instability episodes seen in patients with to normalization of proprioception.glenohumeral instability. Subacromial decompression was also found to restore

Muscle activation abnormalities associated with sub- proprioception in patients with subacromial impinge-acromial impingement and rotator cuff lesions have also ment (Machner et al., 2003). It was suggested that thebeen identified (Ludewig and Cook, 2000; Reddy et al., painful subacromial bursa (and subsequent resection)2000; Kelly et al., 2005). Common findings include was the cause for the initial deficit and subsequentincreased activity in the middle deltoid, decreased restoration of proprioception. These results are sup-activity in the supraspinatus, infraspinatus, and sub- ported by Cuomo et al. (2005) who found that bothscapularis, decreased coactivation of the rotator cuff measures of kinesthesia and joint position sensemusculature, and suppressed scapular stabilization by returned to normal levels following total shoulderthe trapezius and serratus anterior muscles during arthroplasty (Cuomo et al., 2005). It was suggested that: elevation. Kelly et al. (2005) assessed activation of the a decrease in pain afferents with greater mechanorecep-I

rotator cuff during functional tasks and demonstrated tor afferent activity following surgery was the mechan-that patients with symptomatic rotator cuff tears exhibit ism for improved proprioception (Machner et al., 2003;

I activation alterations that may limit functional perfor- Cuomo et al., 2005). Other potential mechanisms forI

200 J.B. Myers et al. / Manua./ Therapy ./ 1 (2006) 197-201

restoration of proprioception following surgery included position (Swanik et al., 2002). Furthermore, both openretensioning of the joint capsule and surrounding and closed kinetic chain exercises have been shown tomusculature, and restoration of anatomical alignment causes improvements in joint position sense at thethrough greater joint congruence following arthroplasty shoulder (Rogol et al., 1998).(Cuomo et al., 2005). It has also been shown that closed kinetic chain upper

As with any injury, rehabilitation should address extremity activities facilitates co-coactivation of theinflammation and pain reduction, a return to normal muscles around the shoulder, increasing functional jointrange of motion and flexibility, and restoration of stability (Ubinger et al., 1999; Henry et al., 2001). Bystrength through traditional rehabilitation exercises. Yet utilizing closed chain exercises, an increase in jointreturn to vigorous physical activity and athletic parti- stability can be obtained by creating greater jointcipation requires additional rehabilitation consider a- congruency and stimulation of articular mechanorecep-tions. Lephart and Henry (1995) promote the use of tors (Ubinger et al., 1999; Henry et al., 2001). There alsofunctional rehabilitation for return to athletic and highly appears to be a central component trained during closeddemanding activities of daily living (Lephart and Henry, chain exercise, as increases were in both shoulders in1996). A large component of functional rehabilitation is subjects training unilaterally (Ubinger et al., 1999).the ability to replicate the demands placed on the joint It has also been shown through a randomizedin a controlled manner to decrease the initial impact controlled trial that enhancing neuromuscular controlupon return to physical activity. Some of the expected through exercises designed to enhance coactivationbenefits of functional rehabilitation include increasing about the shoulder leads to faster recovery of chronicproprioceptive awareness, increasing dynamic stabiliza- shoulder pain than natural course of recovery (Ginn andtion, eliciting preparatory and reactive muscle activa- Cohen, 2005). It was also shown to be equivalent intion, and restoration of functional movement patterns .recovery time as steroid injection and physical mod-(Lephart and Henry, 1996). Proprioceptive awareness alities. The authors advocate retraining as it is more costtraining ins believed to reestablish afferent pathways effective than modalities and has less inherent risk thanfrom the mechanoreceptors a to the central nervous injection (Ginn and Cohen, 2005).system, and facilitate supplementary afferent pathwaysas a compensatory mechanism for proprioceptivedeficits that resulted from joint injury (Myers andLephart, 2000). Dynamic stabilization is paramount in 5. Summaryrestoring functional joint stability and should focus onrestoring both coordinated muscle activation patterns Functional joint stability results from a coordinationduring functional tasks as well as muscle coactivation of both mechanical restraints (provided by capsuloliga-and the resulting force coupling restraint. Elicitation of mentous, articular, and musculotendinous structures)preparatory and reactive muscle activation around the and dynamic restraints that result from contraction ofshoulder helps to establish reflex loops and muscle the musculature that surrounds the joint. Actingstiffness around the joint thus creating stability during independently, neither the mechanical nor dynamicdestabilizing events. To further ease the transition from restraints alone can provide joint stability. There mustrehabilitation to the functional demands of sports or be coordination between the mechanical and dynamicoccupation, allowing controlled simulation of tasks is restraints. The coordination between the mechanicalbeneficial. Recreating the activities which will be and dynamic restraints is mediated by the sensorimotorrequired of the joint during sports in the clinical setting system. The sensorimotor system includes the sensory,allows a controlled environment to practice and evaluate motor, and central integration/processing componentstechniques prior to actual specific performance. of the central nervous system that contribute to joint

There is some evidence of the effectiveness of exercise stability. Sensory information provided by the jointin restoring sensorimotor mechanisms at the shoulder. (proprioception) travels through afferent pathways toShoulder plyometric training has been shown to increase the central nervous system, where it is integrated withproprioception in swimmers (Swanik et al., 2002). It was information from other levels of the nervous system.theorized that repeated eccentric loading and subse- The central nervous system, in turn, elicits efferentquent length/tension changes in the shoulder stabilizers motor responses (neuromuscular control) vital toat end-range of motion, created increased propriocep- coordinated movement patterns and functional stability.tive awareness of by both the mechanical and dynamic With joint injury, not only are the mechanical restraintsstabilizers (Swanik et al., 2002). Additionally, increases disrupted (instability, lesion, etc.) but also, the sensor-in central processing may have resulted from performing imotor system is affected. Demonstrated deficits in boththe repeating, perturbing plyometric tasks. This creates proprioception and neuromuscular control accompanyincreased muscle tension in preparation to the task being joint injury. Both surgical intervention and rehabilita-performed, which may have increased awareness of joint tion have been demonstrated to restore not only theL

J.B. Myers et al. / Manual Therapy II (2006) 197-201 201

mechanical restraints that are disrupted with injury,. but Machner A, Merk H, Becker R, Rohkohl K, Wissel H, Pap G.also the sensorimotor contributors to joint stability. Kinesthetic sense of the shoulder in patients with impingement

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